Prevalence and identification of oral candida species in patients with type 2 diabetes in Yogyakarta

https://doi.org/10.22146/majkedgiind.76176

Dewi Agustina(1*), Regina Titi Chrisnawati(2), Bernadetta Esti Chrismawaty(3), Sri Budiarti Wongsohardjono(4), Fimma Naritasari(5), Andari Sarasati(6)

(1) Department of Oral Medicine, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(2) Department of Oral Biology, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(3) Department of Oral Medicine, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(4) Department of Oral Medicine, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(5) Department of Oral Medicine, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(6) Doctoral Program, Faculty of Dentistry, Universitas Gadjah Mada, Yogyakarta
(*) Corresponding Author

Abstract


Patients with diabetes are prone to recurring and even resistant Candidiasis, making treatment challenging. Many hypotheses proposed related to susceptibility of diabetic patients to Candida. The prevalence and species of Candida in a particular diabetic community might be different compared to other diabetic community. This study aimed to determine the prevalence of Candida colony and its species in the oral cavity of diabetic patients included in the CDM (Chronic Disease Management) program in Yogyakarta. One hundred patients with type 2 diabetes (n= 100) were recruited as the subjects of this study. The subjects were classified into controlled and uncontrolled Diabetes mellitus (DM). Samples of oral rinse solution were collected to determine the species of Candida and number of Candida colonies using CHROMagar Candida medium. There were 47 and 53 of subjects with controlled and uncontrolled DM, respectively. The mean number of Candida colony in the subjects with controlled diabetes (1003.13) was higher than that in the subjects with uncontrolled diabetes (478.43). The Candida colony most commonly identified in the subjects with controlled and uncontrolled diabetes were C. albicans and C. glabrata, respectively. Female patients had higher mean number of Candida colony (859.51) compared to male (299.21). The Candida colony most often identified in both genders was C. albicans. In addition, the subjects of this study consisted of 83 geriatric subjects and 17 non geriatric subjects, in which the mean number of Candida colony in the geriatric subjects (761.77) was higher than that in the non-geriatric subjects (545.71). The Candida colony most often identified in the geriatric subjects and non-geriatric subjects was C. albicans and C. glabrata, respectively. The Mann Whitney test demonstrated that there was a significant difference (p = 0.009) of the mean number of Candida colony between male and female. However, there was no significant difference of the mean number of Candida colony between ages (p = 0.060) and diabetic status (p=0.175). It can be concluded that the Candida species most commonly identified in all the subjects was Candida albicans with the mean colony number of 349.96, followed by C. glabrata (225.97), C. krusei (144.91), C. tropicalis (3.67), and other species (2.02).


Keywords


Candida sp; oral cavity; prevalence; type 2 DM

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References

1. Awad N, Langi YA, Pandelaki K. Gambaran Faktor Resiko Pasien Diabetes Melitus Tipe II
di Poliklinik Endokrin Bagian/SMF FK-Unsrat RSU Prof. Dr. R.D Kandou Manado Periode
Mei 2011 - Oktober 2011. Jurnal e-Biomedik. 2013; 1(1):45–9.

2. Soewondo P, Ferrario A, Levenus Tahapary D. Challenges in diabetes management in
Indonesia: a literature review. Global Health. 2013; 9(63): 1–17. doi: 10.1186/1744-8603-9-63

3. Kementerian Kesehatan RI. Laporan Nasional Riskesdas 2018. Jakarta: Badan Penelitian dan
Pengembangan Kesehatan; 2019. 1: 127–131.

4. Lynnea SB, Inés ÁM, Matildec de B, Andrés C. Candida species and other yeasts in the
oral cavities of type 2 diabetic patients in Cali, Colombia. Colomb Med. 2013; 44(1): 26–30.
doi: 10.25100/cm.v44i1.1040

5. Singh A, Verma R, Murari A, Agrawal A. Oral candidiasis: An overview. Journal of Oral and
Maxillofacial Pathology. 2014; 18(5): 81–85. doi: 10.4103/0973-029X.141325

6. Xiao JL, Xu GC, de Hoog S, Qiao JJ, Fang H, Li YL. Oral prevalence of candida species
in patients undergoing systemic glucocorticoid therapy and the antifungal sensitivity of the
isolates. Infect Drug Resist. 2020; 13: 2601–2607. doi: 10.2147/IDR.S262311

7. Silva JJ da, Silva TA da, Almeida H de, Rodrigues Netto MF, Cerdeira CD, Höfling JF,
Boriollo MFG. Candida species biotypes in the oral cavity of infants and children with orofacial
clefts under surgical rehabilitation. Microb Pathog. 2018; 124: 203–215.
doi: 10.1016/j.micpath.2018.08.042

8. Yang B, Rao R. Emerging Pathogens of the Candida Species. In: Candida Albicans.
IntechOpen; 2019. 1–16. doi: 10.5772/intechopen.80378

9. Verhulst MJL, Loos BG, Gerdes VEA, Teeuw WJ. Evaluating all potential oral complications
of diabetes mellitus. Front Endocrinol (Lausanne). 2019; 10(56): 1–49.
doi: 10.3389/fendo.2019.00056

10. Bhattacharyya A, Chandra S, Singh A, Raj V, Gupta B. Salivary glucose levels and oral
candidal carriage in Type 2 diabetics. J Oral Biol Craniofac Res. 2018; 8(3): 158–164.
doi: 10.1016/j.jobcr.2016.11.004

11. Rodrigues CF, Rodrigues ME, Henriques M. Candida sp. Infections in patients with
diabetes mellitus. J Clin Med. 2019; 8(1): 1–41. doi: 10.3390/jcm8010076

12. Dehghan P, Mohammadi F, Javaheri MR, Nekoeian S. Identification of Candida species
in the oral cavity of diabetic patients. Curr Med Mycol. 2016; 2(2): 0–0.
doi: 10.18869/acadpub.cmm.2.2.4

13. Darwazeh AMG, Darwazeh TA. What makes oral candidiasis recurrent infection? a clinical
view. J Mycol. 2014; 2014: 1–5. doi: 10.1155/2014/758394

14. Chouhan S, Kallianpur S, Prabhu Kt, Tijare M, Kasetty S, Gupta S. Candidal prevalence
in diabetics and its species identification. Int J Appl Basic Med Res. 2019; 9(1): 49–54.
doi: 10.4103/ijabmr.ijabmr_259_18

15. Anil Kumar D, Muralidhar S, Biswas K, Banerjee U, Basir SF, Khan LA. Species
diversity, antifungal susceptibility, and virulence attributes of candida colonising the
oral cavities of adult diabetic patients. J Mycol. 2014; 2014(395041): 1–9.
doi: 10.1155/2014/395041

16. Nikbin A, Bayani M, Jenabian N, khafri S, Motallebnejad M. Oral health-related quality
of life in diabetic patients: comparison of the persian version of geriatric oral health
assessment index and oral health impact profile: a descriptive-analytic study. J Diabetes
Metab Disord. 2014; 13(1): 32. doi: 10.1186/2251-6581-13-32

17. González-Moles MÁ, Ramos-García P. State of evidence on oral health problems in diabetic
patients: A critical review of the literature. J Clin Med. 2021; 10(22): 5383.
doi: 10.3390/jcm10225383

18. Agustina D, Purwanti N, Hanindriyo L, Naritasari F. Oral health-related quality of
life in type 2 diabetic patients of Yogyakarta General Hospital. Majalah Kedokteran Gigi
Indonesia. 2021; 7(1): 1-9. doi: 10.22146/majkedgiind.43693

19. Ahmad R, Haque M. Oral health messiers: Diabetes mellitus relevance. Vol. 14, Diabetes,
Metabolic Syndrome and Obesity: Targets and Therapy. Dove Medical Press Ltd; 2021.
3001–3015. doi: 10.2147/DMSO.S318972

20. Petrovic SM, Radunovic M, Barac M, Pficer JK, Pavlica D, Arsenijevic VA, Pucar A.
Subgingival areas as potential reservoirs of different Candida spp in type 2 diabetes
patients and healthy subjects. PLoS One. 2019; 14(1): 1–14.
doi: 10.1371/journal.pone.0210527

21. Samnieng P, Sonthayasathapon S, Siriwat M, Jeamanukulkit S. A cross-sectional study of
the candidal species isolated in the a crosssectional study of the candidal species isolated
in the oral cavities of type II diabetic patients oral cavities of type II diabetic patients a crosssectional study of the candidal species isolated in the oral cavities of type II diabetic patients. Makara Journal of Health Research. 2017; 21(3): 99–103. doi: 10.7454/msk.v21i3.7220

22. Suhartono S, Mahdani W, Masthura A, Rusmana I. Candida species distribution of
clinical specimens in Banda Aceh, Indonesia. Biosaintifika: Journal of Biology & Biology
Education. 2020; 12(2): 262–267. doi: 10.15294/biosaintifika.v12i2.23758

23. Nugraha A, Savitri D, Sosiawan A. Prevalence of candida species in oral candidiasis and
correlation with CD4+ count in HIV/AIDS patients at surabaya, Indonesia. Article in
Journal of International Dental and Medical Research. 2018; 11(1): 81–85.

24. Man A, Ciurea CN, Pasaroiu D, Savin AI, Toma F, Sular F, Santacroce L, Mare A.
New perspectives on the nutritional factors influencing growth rate of Candida albicans in
diabetics. An in vitro study. Mem Inst Oswaldo Cruz. 2017; 112(9): 587–592.
doi: 10.1590/0074-02760170098

25. Wulandari A, Hapsari R, Sari D, Puspitasari I, Tugasworo Pramukarso D. Antifungal
susceptibility profile of Candida spp. causing candidemia in an Indonesian tertiary hospital.
Journal of Clinical Microbiology and Infectious Diseases. 2021; 1(1): 28-32.

26. UNFPA Indonesia. Indonesia on the Threshold of Population Ageing. 1st ed. Posselt H, editor.
Vol. 1. Jakarta: United Nations Population Fund; 2014. 1–10.

27. Cheng X, Yang Y, Schwebel DC, Liu Z, Li L, Cheng P, Hu G. Population ageing and mortality
during 1990-2017: A global decomposition analysis. PLoS Med. 2020; 17(6): 1–17.
doi: 10.1371/journal.pmed.1003138

28. Badan Pusat Statistik. Statistik Penduduk Lanjut Usia 2012. 1st ed. Chamami A, editor.
Vol. 4104001. Jakarta: Badan Pusat Statistik, Jakarta-Indonesia; 2012. 25–32.

29. World Health Organization. Women, Ageing and Health: A Framework for Action. 1st ed.
Vol. 1. Geneva: WHO Library Cataloguing-in-Publication Data; 2007. 1–3.

30. Muthuveera Ganapathy D, Joseph S, Ariga P, Selvaraj A. Evaluation of the influence
of blood glucose level on oral candidal colonization in complete denture wearers with
Type-II Diabetes Mellitus: An in vivo Study. J Dent Res. 2013; 10(1): 87-92.
doi: 10.4103/1735-3327.111806

31. Nurmansyah D, Stasya E, Ramadhani D, Normaidah N, Astuti A. Hyperglicemia as
predisposition factor of oral candidiasis on patient with diabetes mellitus. Biomedika.
2020; 13(1): 46–50. doi: 10.31001/biomedika.v13i1.703

32. Matić-Petrović S, Barać M, Kuzmanović-Pfićer J, Radunović M, Jotić A, Pucar A. Presence of
different Candida species at denture wearers with type 2 diabetes and clinically healthy oral
mucosa: Pilot study. Balkan Journal of Dental Medicine. 2018; 22(3): 15–21.
doi: 10.2478/bjdm-2018-0003

33. Al-Maweri SA, Altayyar MO, Alqahtani KW, Bamasud MS, Alghamdi OY, Ashraf S, Eshky
R, Ba-Hattab R, Kassim S. Xerostomia, salivary flow, and oral health status among saudi diabetic
patients: A comparative cross-sectional study. Clin Cosmet Investig Dent. 2021; 13: 451–458.
doi: 10.2147/CCIDE.S337581

34. Bhuyan L, Hassan S, Dash K, Panda A, Behura S, Ramachandra S. Candida species diversity
in oral cavity of type 2 diabetic patients and their in vitro antifungal susceptibility. Contemp
Clin Dent. 2018; 9(5): S83–S88. doi: 10.4103/ccd.ccd_70_18

35. Reinhardt LC, da Silva Nascente P, Ribeiro JS, Etges A, Lund RG. A single-center 18-
year experience with oral candidiasis in Brazil: a retrospective study of 1,534 cases. Braz
Oral Res. 2018; 32(e92): 1–8. doi: 10.1590/1807-3107bor-2018.vol32.0092

36. Kumwenda P, Cottier F, Hendry AC, Kneafsey D, Keevan B, Gallagher H, Tsai HJ, Hall RA.
Estrogen promotes innate immune evasion of Candida albicans through inactivation of the
alternative complement system. Cell Rep. 2022; 38(1): 1–9.
doi: 10.1016/j.celrep.2021.110183

37. Disha T, Haque F. Prevalence and risk factors of vulvovaginal candidosis during pregnancy:
a review. Infect Dis Obstet Gynecol. 2022; 2022(6195712): 1–14. doi: 10.1155/2022/6195712

38. Loster JE, Wieczorek A, Loster BW. Correlation between age and gender in Candida species
infections of complete denture wearers: A retrospective analysis. Clin Interv Aging. 2016;
11:1707–14. doi: 10.2147/CIA.S116658

39. Byadarahally Raju S, Rajappa S. Isolation and identification of candida from the oral cavity.
ISRN Dent. 2011; 2011: 1–7. doi: 10.5402/2011/487921

40. Alrayyes SF, Alruwaili HM, Taher IA, Elrahawy KM, Almaeen AH, Ashekhi AO, et
al. Oral Candidal carriage and associated risk indicators among adults in Sakaka, Saudi
Arabia. BMC Oral Health. 2019; 19(1). doi: 10.1186/s12903-019-0775-8

41. Kean R, Delaney C, Rajendran R, Sherry L, Metcalfe R, Thomas R, McLean W, Williams C, Ramage G. Gaining insights from Candida biofilm heterogeneity: One size does not fit all. Journal of Fungi. 2018; 4(1): 1–20. doi: 10.3390/jof4010012

42. Vipulanandan G, Herrera M, Wiederhold NP, Li X, Mintz J, Wickes BL, Kadosh D. Dynamics of
Mixed–Candida Species Biofilms in Response to Antifungals. J Dent Res. 2018; 97(1): 91–
98. doi: 10.1177/0022034517729351

43. Sherry L, Rajendran R, Lappin DF, Borghi E, Perdoni F, Falleni M, Tosi D, Smith K,
Williams C, Jones B, Nile CJ, Ramage G. Biofilms formed by Candida albicans bloodstream isolates display phenotypic and transcriptional heterogeneity that are associated with resistance and pathogenicity. BMC Microbiol. 2014; 14(1): 182. doi: 10.1186/1471-2180-14-182

44. Felipe Fernandez Martinez R, Jaimes-Aveldañez A, Hernández-Pérez F, Arenas
R, Fabián G, Miguel S. Oral Candida spp carriers: its prevalence in patients with type
2 Diabetes Mellitus. An Bras Dermatol. 2013; 88(2): 222–227.
doi: 10.1590/S0365-05962013000200006

45. Mayer FL, Wilson D, Hube B. Candida albicans pathogenicity mechanisms. Virulence. 2013;
4(2): 119–28. doi: 10.4161/viru.22913



DOI: https://doi.org/10.22146/majkedgiind.76176

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